染色質(zhì)重塑因子在植物發(fā)育過程的功能

彭銹玲, 王劍豪, 楊松光

染色質(zhì)重塑因子在植物發(fā)育過程的功能

彭銹玲1,2, 王劍豪1,2, 楊松光1*

(1. 中國科學(xué)院華南植物園, 華南農(nóng)業(yè)植物分子分析與遺傳改良重點(diǎn)實(shí)驗(yàn)室，廣州 510650; 2. 中國科學(xué)院大學(xué), 北京 100049)

染色質(zhì)重塑復(fù)合體(chromatin remodeling complexes)通過具有ATPase活性的亞基水解ATP釋放能量，通過改變核小體“構(gòu)象”(包括核小體重定位、核小體滑動(dòng)和核小體替換等)而改變DNA的“可及性”(accessibility)，進(jìn)而影響特定的生理、生化過程。染色質(zhì)重塑復(fù)合體最早在酵母中發(fā)現(xiàn)，生化分析表明其至少含有13個(gè)亞基。目前植物染色質(zhì)重塑復(fù)合體的組成還未完全解析，但通過對(duì)其酵母同源亞基(染色質(zhì)重塑因子)的研究可從側(cè)面探究植物染色質(zhì)重塑復(fù)合體的功能。同時(shí)，還著重討論了近年來在植物染色質(zhì)重塑因子研究上取得的結(jié)果，以期為植物染色質(zhì)重塑的作用機(jī)制提供啟示。

染色質(zhì)重塑因子；表觀調(diào)控；功能；植物

1 染色質(zhì)重塑復(fù)合體

真核生物遺傳信息以核小體為基本單位，經(jīng)高度包裹壓縮存儲(chǔ)于染色質(zhì)中。因此真核生物在DNA復(fù)制、轉(zhuǎn)錄、重組和DNA修復(fù)等過程中首先要克服DNA與組蛋白之間的“緊密”結(jié)合。涉及該過程的蛋白主要包括兩類，即染色質(zhì)修飾酶(包括組蛋白修飾酶和DNA修飾酶)和依賴于ATP的染色質(zhì)重塑因子(ATP-dependent chromatin remodelers, ATPase)。前者通過添加或者移除組蛋白和DNA上的化學(xué)基團(tuán)改變DNA的“可及性”[1]，而后者通過與其他蛋白組成染色質(zhì)重塑復(fù)合體水解ATP釋放能量，改變核小體“構(gòu)象”(positioning, occupancy and composition of nucleosomes)而改變DNA的“可及性”，進(jìn)而影響特定的生理過程[2–3]。

染色質(zhì)重塑復(fù)合體最早從酵母()和(sucrose non-fermenting)突變體中分離鑒定。生化分析表明該復(fù)合體含有至少11個(gè)亞基(SWI1、SWI2/SNF2、SWI3、SNF5、SWP73、ARP7、ARP9、SWP82、SNF6、SNF11和TAF14)，其中SWI2/SNF2蛋白具有ATPases活性[4]，SWP82、SNF6、SNF11和TAF14為酵母所特有(表1)。根據(jù)ATPase亞基的結(jié)構(gòu)，可將染色質(zhì)重塑復(fù)合體分為4類(表1~3)，即SWI/SNF、ISWI、CHD和INO80/SWR1[2], 且不同復(fù)合體可能包括相同的亞基。研究表明，這4類染色質(zhì)重塑復(fù)合體ATPase亞基無論是在酵母、果蠅還是人類中均十分保守，含有保守的ATPase催化結(jié)構(gòu)域(SNF2-N結(jié)構(gòu)域)，該催化結(jié)構(gòu)域可進(jìn)一步細(xì)分為DExx和HELICc兩部分(圖1)。除ATPase催化結(jié)構(gòu)域外，不同染色質(zhì)重塑復(fù)合體ATPase亞基還含有特異結(jié)構(gòu)，如SWI/SNF (matingtype switching/sucrose non-fermenting)復(fù)合體ATPase亞基N端含有HSA (helicase-SANT)結(jié)構(gòu)域而C端含有bromodomain結(jié)構(gòu)域[5–6]。bromodomain結(jié)構(gòu)域能識(shí)別組蛋白“尾巴”乙?；臍埢?，使SWI/SNF復(fù)合體結(jié)合在染色質(zhì)特定位點(diǎn)[7–8]。而ISWI (imitation switch)復(fù)合體ATPase亞基C端含有SANT和SLIDE結(jié)構(gòu)域，這二者形成一個(gè)核小體識(shí)別結(jié)構(gòu)與未修飾的組蛋白和DNA結(jié)合[9]。CHD (chromodomain helicase-DNA binding)復(fù)合體ATPase亞基N端有串聯(lián)的chromodomain結(jié)構(gòu)域[10]，能識(shí)別組蛋白H3K4的甲基化位點(diǎn)[11–12]。與其他三類ATPase亞基相比，INO80/SWR1 (inositol requiring 80)復(fù)合體ATPase亞基結(jié)構(gòu)域DExx與HELICc之間有一段較長的氨基酸殘基(圖1)，然而這并未影響其ATPase的活性[13]。

表1 不同物種的SWI/SNF復(fù)合體組成

表2 不同物種的ISWI、CHD復(fù)合體組成

表3 不同物種INO80/SWR1復(fù)合體組成

雖然不同染色質(zhì)重塑復(fù)合體ATPase亞基在結(jié)構(gòu)上較為保守，但不同染色質(zhì)重塑復(fù)合體具有特有的功能。如ISWI和CHD復(fù)合體主要參與DNA復(fù)制后染色質(zhì)的組裝[14]；而SWI/SNF復(fù)合體則影響染色質(zhì)的去組裝和核小體穩(wěn)定蛋白的替換[15–17]。INO80/SWR1復(fù)合體則介導(dǎo)組蛋白變體(histonevariant)的替換，其中INO80復(fù)合體介導(dǎo)H2A替換H2A.Z，而SWR1復(fù)合體則與之相反[18–20]。組蛋白H2A與組蛋白變體H2A.Z之間的互換對(duì)核小體結(jié)構(gòu)穩(wěn)定性至關(guān)重要[21–23]。

圖1 不同染色質(zhì)重塑復(fù)合體ATPase亞基結(jié)構(gòu)示意圖(引自Clapier[2])

目前對(duì)染色質(zhì)重塑復(fù)合體的作用機(jī)制并不十分清楚。一般認(rèn)為，染色質(zhì)重塑復(fù)合體ATPase亞基與DNA易位酶(DNA translocases)具有相似之功能。當(dāng)染色質(zhì)重塑復(fù)合體ATPase亞基與核小體結(jié)合后，其易位酶活性將核小體之間的連接DNA (linker)推向核小體核心結(jié)構(gòu)，使DNA形成一個(gè)環(huán)狀結(jié)構(gòu)(loop)，從而使DNA與組蛋白之間結(jié)合由“緊密”狀態(tài)變?yōu)椤八缮ⅰ睜顟B(tài)[24–27]。該過程可能同時(shí)產(chǎn)生很多環(huán)狀結(jié)構(gòu)，這些環(huán)狀結(jié)構(gòu)只需改變DNA與1~2個(gè)組蛋白的結(jié)合程度即可啟動(dòng)核小體的滑動(dòng)。然而，對(duì)形成的環(huán)狀結(jié)構(gòu)大小并不十分清楚, 目前的證據(jù)支持該環(huán)狀結(jié)構(gòu)可能由較多的堿基(約100 bp)組成[28]。而關(guān)于染色質(zhì)重塑是如何被精確調(diào)節(jié)的還知之甚少，該過程可能與組蛋白的翻譯后修飾有關(guān)。如H4尾巴第17~19位殘基乙?；芴岣唧蛤?) ISWI復(fù)合體催化活性[29–30],而H4K16ac則抑制其活性。對(duì)酵母yISW2 (ISWI復(fù)合體催化亞基)和yChd1 (CHD復(fù)合體催化亞基)而言，H4乙酰化抑制其ATPase活性而不響應(yīng)它與核小體結(jié)合，然而H4乙酰化卻能提高酵母RSC復(fù)合體(SWI/SFN類)的重塑活性[31]。

2 植物染色質(zhì)重塑因子及功能

目前，植物染色質(zhì)重塑復(fù)合體組成尚未完全分離鑒定，然而遺傳和蛋白相互作用數(shù)據(jù)提示植物中也存在多種染色質(zhì)重塑復(fù)合體(表1~3)。因此通過對(duì)染色質(zhì)重塑復(fù)合體同源亞基的研究可從側(cè)面探究植物染色質(zhì)重塑復(fù)合體的功能。通過與酵母、果蠅和人的染色質(zhì)重塑復(fù)合體ATPase亞基的同源比對(duì)，擬南芥含41個(gè)ATPase結(jié)構(gòu)域(SNF2-like)基因，可分為Snf2-like、Swr1-like、Rad54-like、Rad5/16-like、SSO1653-like和SMARCAL1-like家族，每個(gè)家族又可細(xì)分為不同亞家族[32]，如Snf2-like家族可分為SWI2/SNF2、Lsh、Iswi、Chd1和Mi-2亞家族，而Swr1-like家族則可分為Ino80、Swr1和Etl1亞家族。遺傳和蛋白相互作用及IP-MS研究表明，擬南芥() SWI/SNF染色質(zhì)重塑復(fù)合體亞基核心組分與酵母和動(dòng)物相似，但含有更多同源基因(如與酵母SWI3同源的SWI3A/B/C/D)，且有植物特有的亞基(圖2)。這提示植物染色質(zhì)重塑復(fù)合體可能具有與動(dòng)物和酵母不同的功能。圍繞各組成亞基的研究表明，這些基因參與細(xì)胞分化、器官發(fā)育和激素信號(hào)轉(zhuǎn)導(dǎo)等多種生理過程(表4)。在擬南芥所有SNF2-N蛋白中Snf2-like (11個(gè))和Swr1-like (4個(gè))家族成員在序列上最有可能是植物染色質(zhì)重塑復(fù)合體催化亞基，圍繞這些基因所取得的研究成果也最豐富。在Snf2-like家族中，SWI2/SNF2亞家族(4個(gè))、CHD1-Mi2亞家族(4個(gè))、Iswi-Lsh亞家族(3個(gè))和Swr1-like家族(4個(gè))成員分別對(duì)應(yīng)于SWI/SNF、CHD、 ISWI和 INO80/SWR1復(fù)合體催化亞基(表1~3)。

圖2 植物SWI/SNF染色質(zhì)重塑復(fù)合體可能組成(修改自Jerzmanowski[33])

2.1 SWI/SNF復(fù)合體

2.1.1 SWI/SNF復(fù)合體催化亞基

SWI/SNF復(fù)合體最早從酵母()中分離鑒定，隨后發(fā)現(xiàn)該類復(fù)合體亦廣泛存在于動(dòng)物如果蠅()、小鼠()和人類中。目前關(guān)于植物SWI/SNF復(fù)合體的具體組成還不十分清楚，但遺傳和蛋白相互作用數(shù)據(jù)顯示該復(fù)合體也存在于植物中。在擬南芥41個(gè)ATPase結(jié)構(gòu)域(SNF2-like)蛋白中，SWI2/SNF2亞家族成員AtBRM (BRAHMA)、AtSYD (SPLAYED)、AtCHR23 (CHROMATINREMODELL ING23)和AtCHR12 (CHROMATIN REMODELL ING 12)最有可能是植物SWI/SNF復(fù)合體催化亞基，其中AtBRM的可能性最大。首先，僅有AtBRM蛋白C-端具有與酵母SWI2/SNF2和果蠅BRAHMA蛋白一樣的bromo結(jié)構(gòu)域；其次，AtBRM蛋白N-端能與酵母SWI3同源蛋白AtSWI3B和AtSWI3C相互作用；最后和突變體具有相似表型[34]。

表4 擬南芥染色質(zhì)重塑因子的功能分析

續(xù)表(Continued)

主要在分生組織和幼嫩器官中表達(dá)，其功能缺失導(dǎo)致2 000余基因中的一半下調(diào)而另一半上調(diào)表達(dá)[104]，這表明具有雙重功能。敲減的植株矮小，在長日照下葉片卷曲，花器官發(fā)育異常；在長日照和短日照下均出現(xiàn)早花現(xiàn)象[33]。缺失突變體中，有相當(dāng)一部分植株在短日照下不開花，這提示在擬南芥開花過程的作用十分復(fù)雜[35]。進(jìn)一步研究表明，除了影響光周期響應(yīng)基因的表達(dá)外，還抑制和的表達(dá)[104–105]。在葉片中，AtBRM分別與TCP4和AN- GUSTIFOLIA3 (AN3)相互作用，共同調(diào)控葉片發(fā)育相關(guān)基因的表達(dá)[38–39]。我們的研究表明，在花序軸中AtBRM與轉(zhuǎn)錄因子BREVIPEDICELLUS (BP)相互作用，直接調(diào)節(jié)和的表達(dá)來調(diào)控花序軸發(fā)育[36]。在黑暗中，AtBRM與PHY-INTER- ACTING FACTOR 1 (PIF1)相互作用抑制()表達(dá)從而抑制葉綠素合成[40]。除轉(zhuǎn)錄因子外, AtBRM亦可與其他核蛋白相互作用。如熱脅迫記憶激活因子FORGETTER1 (FGT1)與AtBRM相互作用，維持下游熱脅迫相關(guān)基因處于轉(zhuǎn)錄激活狀態(tài)[42]。而植物H3K27去甲基化酶RELATIVE OF EARLY FLO- WERING 6 (REF6)通過招募AtBRM結(jié)合于下游基因CTCTGYTY基序降低其H3K27me3水平激活轉(zhuǎn)錄[41]。這與動(dòng)物中BRM拮抗PcG蛋白(polycomb group proteins)的作用一致。PcG蛋白作為表觀遺傳抑制因子維持細(xì)胞內(nèi)非活化基因的抑制狀態(tài)，其分別通過與Polycomb Repressive Complex 1 (PRC1) 和PRC2復(fù)合體相互作用建立和維持染色質(zhì)抑制狀態(tài)。PRC2復(fù)合體與目標(biāo)基因結(jié)合后，催化這些基因組蛋白H3K27me3修飾，從而抑制基因表達(dá)。這與我們?cè)跀M南芥主根發(fā)育過程觀察到AtBRM拮抗PcG蛋白影響生長素運(yùn)輸?shù)鞍谆虮磉_(dá)，從而影響主根根冠干細(xì)胞微環(huán)境維持的結(jié)果一致[43]。最近研究表明，翻譯后修飾對(duì)染色質(zhì)重塑過程也起著重要作用，AtBRM作為ABA信號(hào)途徑核心組分SnRK (蔗糖非依賴1蛋白激酶)和PP2C (蛋白磷酸酶2C)的底物來調(diào)控ABA反應(yīng)[46]；我們亦觀察到，METHYL METHANE SULFONATE SENSITIVITY 21 (MMS21)通過SUMO化修飾AtBRM調(diào)節(jié)其蛋白穩(wěn)定性參與主根發(fā)育[43]。有趣的是，新的研究結(jié)果表明microRNA前體(pri-miRNAs)也能與AtBRM相互作用，AtBRM作為microRNA前體加工復(fù)合體SE (MICROPRO CESSOR COMPONENT SERRATE)組分改變microRNA前體二級(jí)結(jié)構(gòu)以便后續(xù)通過DCL1和HYL1進(jìn)一步加工[47]。

對(duì)擬南芥SWI2/SNF2亞家族其他成員的研究表明，參與頂端分生組織(SAM)活性的維持。缺失突變體植株矮小，生長緩慢、葉片極性和SAM缺失。其作用機(jī)理是，通過途徑影響SAM的維持，因?yàn)锳tSYD可與BARD1相互作用結(jié)合于啟動(dòng)子直接結(jié)合而調(diào)節(jié)表達(dá), 后者促進(jìn)SAM中干細(xì)胞活性[48–49]。進(jìn)一步研究還表明，AtSYD通過調(diào)控JA和ET信號(hào)相關(guān)基因參與植物的生物脅迫響應(yīng)[106]，而這種脅迫大部分是通過抑制(SUPPRESSOR OF NPR1, CONSTITU- TIVE 1)實(shí)現(xiàn)的[107]。對(duì)和在植物發(fā)育中的功能還不十分清楚。過表達(dá)和均抑制植物種子萌發(fā)[50]，在其他發(fā)育過程過表達(dá)顯著抑制植物生長，而過表達(dá)表型則不明顯[51]；但在脅迫方面, 二者表型相似[52–53]。

2.1.2 SWI/SNF復(fù)合體非催化亞基-SWI3類蛋白

擬南芥基因組編碼4個(gè)SWI3同源蛋白，分別為AtSWI3A、AtSWI3B、AtSWI3C和AtSWI3D, 在結(jié)構(gòu)上他們均含有SWIRM、SANT和Leucine Zipper 結(jié)構(gòu)域。進(jìn)化分析表明植物SWI3類蛋白可明顯分為兩簇，即SWI3A/B和SWI3C/D，這也與AtSWI3A、AtSWI3B、AtSWI3C和AtSWI3D的生物學(xué)功能有所差異相符。與突變導(dǎo)致植物胚在早期發(fā)育過程異常，而和突變使得植物葉片和花器官發(fā)育異常[53]。有意思的是突變還導(dǎo)致植物主根發(fā)育異常，而其他3個(gè)突變體則未觀察到相應(yīng)表型[53]。酵母雙雜交結(jié)果表明，AtSWI3A可分別與AtSWI3A、AtSWI3B、AtSWI3C、BSH、AtSYD和FCA相互作用[53–54], 提示AtSWI3A、BSH和AtSYD可能形成1個(gè)復(fù)合體。然而關(guān)于AtSWI3A與其他蛋白相互作用的生物學(xué)意義目前并不清楚。對(duì)AtSWI3B而言，除分別可與AtSWI3A、AtSWI3B、AtSWI3C、AtSWI3D、BSH、AtSYD、AtBRM相互作用外, 還分別與type 2C類磷酸酶(phosphatase type 2C) HAB1 (HYPERSENSI- TIVE TO ABA1)和長鏈非編碼RNA結(jié)合蛋白IDN2相互作用，參與ABA信號(hào)和長鏈非編碼RNA形成[55–56]。進(jìn)一步研究還表明，AtSWI3B (包括At- SWI3C和AtSWI3D)與MORC6 (microrchidia 6)、SUVH9 [SU(VAR)3-9 homolog]和IDN2形成復(fù)合體, 通過RNA指導(dǎo)的DNA甲基化(RdDM, RNA-directedDNA methylation)介導(dǎo)的途徑調(diào)控DNA的甲基化[57]。在葉片發(fā)育過程,通過調(diào)控生長素代謝酶基因(IAA carboxyl methyltransferase 1)的染色質(zhì)“構(gòu)象”調(diào)節(jié)其表達(dá)，從而參與葉片發(fā)育[58]。

AtSWI3C也分別與AtSWI3A、AtSWI3B、AtSYD和AtBRM相互作用，進(jìn)一步研究表明其還可與轉(zhuǎn)錄因子AN3和酵母SWI/SNF復(fù)合體同源蛋白SWP73B以及ARP4/7 (actin-related protein4/7)相互作用調(diào)控葉片發(fā)育[39]。同時(shí)，AtSWI3C通過與DELLA蛋白R(shí)GL2和RGL3相互作用促進(jìn)(GIBBERELLIN-INSENSITIVE DWARF1)和(GIBBERELLIN 3-OXIDASE)表達(dá)，參與GA信號(hào)轉(zhuǎn)導(dǎo)[59]。相對(duì)于其他3個(gè)AtSWI3蛋白，AtSWI3D的功能還知之甚少，其缺失植株的表型與和缺失突變體相似，出現(xiàn)葉片卷曲，花器官發(fā)育異常和育性降低等表型[53]。

2.1.3 SWI/SNF復(fù)合體非催化亞基-SNF5類蛋白

4.4.2 強(qiáng)化服務(wù)監(jiān)督，完善管理制度。進(jìn)一步完善和優(yōu)化項(xiàng)目立項(xiàng)制、項(xiàng)目公示制、項(xiàng)目審計(jì)制、項(xiàng)目檢查驗(yàn)收制、后續(xù)管護(hù)等制度，加強(qiáng)項(xiàng)目事中、事后監(jiān)督。

在酵母中，SNF5蛋白對(duì)染色質(zhì)的裝配和基因啟動(dòng)子與SWI/SNF復(fù)合體的結(jié)合至關(guān)重要[108]，其C端保守的200個(gè)氨基酸殘基形成兩個(gè)重復(fù)結(jié)構(gòu)負(fù)責(zé)與SWI/SNF復(fù)合體其他亞基和其他因子如cyclin E/CDK2之間的相互作用。動(dòng)物發(fā)生突變往往會(huì)導(dǎo)致癌癥。在擬南芥中，SNF5同源蛋白BSH(BUSHY GROWTH)僅由1個(gè)基因編碼，其可與AtSWI3A和AtSWI3B相互作用，且在酵母中異源表達(dá)，可互補(bǔ)酵母突變體表型[61]。利用反義RNA技術(shù)降低表達(dá)導(dǎo)致植物頂端分生組織減小且出現(xiàn)不育表型[61]。T-DNA插入突變體雖然導(dǎo)致種子貯存基因在幼苗中異位表達(dá)，然而植株卻未出現(xiàn)可以看到的表型[60]。這可能是由于T-DNA插入位置在BSH的C端，僅破壞BSH蛋白C端結(jié)構(gòu)使得BSH還保留部分功能。

2.1.4 SWI/SNF復(fù)合體非催化亞基SWP73類蛋白

酵母SWI/SNF復(fù)合體亞基SWP73對(duì)SWI/SNF復(fù)合體在轉(zhuǎn)錄過程的作用至關(guān)重要。在植物中，擬南芥基因組編碼兩個(gè)SWP73蛋白：SWP73A和SWP73B，二者氨基酸序列相似度高達(dá)83.7%。蛋白互作分析表明SWP73A僅可與AtSWI3C相互作用，而SWP73B不僅可以與AtSWI3C和AtSWI3D相互作用，還能與AtBRM和ARP4/7以及轉(zhuǎn)錄因子AN3相互作用[39]。生物學(xué)功能分析表明，和功能亦有所差異，突變植物未出現(xiàn)可見表型，而突變導(dǎo)致植物根[63]、葉片和花發(fā)育異常[62]和開花時(shí)間推遲[64]。進(jìn)一步研究表明，通過促進(jìn)根中細(xì)胞分裂素的合成促進(jìn)根中分生組織的維持[63]；同時(shí)通過改變?nèi)旧|(zhì)組蛋白修飾水平和H2A.Z的替換影響表達(dá)從而參與植物成花控制[64]。最新的研究表明，SWP73B通過直接結(jié)合于下游基因的G-box區(qū)域調(diào)節(jié)其表達(dá)抑制下胚軸伸長，但與SWP73B直接結(jié)合的基因與PIF4結(jié)合的基因大部分是不同的[65]。在脅迫方面,還參與UV-B介導(dǎo)的DNA損傷修復(fù)，然而其作用機(jī)制還不清楚[66]。

2.1.5 SWI/SNF復(fù)合體非催化亞基ARP類蛋白

酵母和動(dòng)物SWI/SNF類復(fù)合體均含有一類ARPs (actin-related proteins)蛋白。在酵母中，ARPs一共有10個(gè)(ARP1~10)，其序列與酵母actin相似性按編號(hào)遞減。在酵母所有ARPs中，ARP7和ARP9是SWI/SNF類(包括RSC)復(fù)合體組分，而ARP4、ARP5和ARP8為INO80/SWR1復(fù)合體組分。動(dòng)物SWI/SNF類僅含有一個(gè)ARP (Baf53/BAP55)，與酵母ARP4同源。雖然在結(jié)構(gòu)上ARPs與actin相似均含有ATP/ADP-binding pocket (actin fold)結(jié)構(gòu)，但除ARP4外，其他所有ARPs均沒有像actin那樣的ATPase活性。生物界所有ARPs可分為11類，其中ARP4~ARP9家族成員大多定位于細(xì)胞核[107]。擬南芥基因組編碼9個(gè)ARPs (ARP2~ARP9，其中ARP4包含2個(gè)同源基因和)，其中ARP4~ ARP9定位于細(xì)胞核[111]。CoIP-MS分析表明在擬南芥所有ARPs中, ARP4和ARP7為SWI/SNF復(fù)合體組分[39]，而后續(xù)的研究表明ARP4也是INO80/ SWR1復(fù)合體的組分。

雖然在正常情況下，ARP4和ARP7定位于細(xì)胞核，但在有絲分裂過程，它們與染色質(zhì)組裝無關(guān),且也可以定位于細(xì)胞質(zhì)[109]。與相似，缺失突變導(dǎo)致植物不育，敲減突變體使植株生長發(fā)育受阻并出現(xiàn)早花、花衰老推遲和花器官發(fā)育異常等表型[67–68]。

2.2 INO80/SWR1復(fù)合體

基因最早從篩選調(diào)控酵母磷脂生物合成的突變體中分離，后續(xù)生化分析表明其與其他14個(gè)亞基組成復(fù)合體(表3)。隨后，同源基因亦在酵母中發(fā)現(xiàn)，其主要催化組蛋白變體Htz1與H2A之間的交換。進(jìn)一步研究表明，也與其他蛋白形成復(fù)合體，其中Rvb1、Rvb2、Arp4和actin亞基與INO80復(fù)合體共有(表3)。擬南芥中編碼4個(gè)(包括PIE1、INO80、CHR19和CHR10)與INO80和Swr1類復(fù)合體催化亞基同源蛋白，目前僅對(duì)CHR19、INO80和PIE1的功能有所了解。

目前的研究認(rèn)為擬南芥SWR1復(fù)合體最少由10個(gè)亞基組成(PIE1、SWC2、SWC4、SWC6、YAF9A、RVB1、RVB2A、RVB2B、ARP4和ARP6)，其中PIE1是催化亞基[73]，首先，PIE1可與SWC2、SWC6和ARP6以及組蛋白H2A相互作用調(diào)控植物開花和發(fā)育[73–74]；其次，與PIE1形成的復(fù)合體在植物調(diào)節(jié)基因表達(dá)過程中也負(fù)責(zé)H2A.Z變體的交換[75–77]。然而有意思的是，在植物免疫過程中，和突變導(dǎo)致植物基本抗性降低，而突變則增加抗性[76]，這提示在不同的生理過程中植物SWR1復(fù)合體亞基的功能可能是不一樣的。進(jìn)一步研究表明，通過促進(jìn)和表達(dá)，抑制二者目標(biāo)基因表達(dá)參與植物發(fā)育[77]。

對(duì)植物INO80/SWR1復(fù)合體非催化亞基RVB1、RVB2A和RVB2B的功能還知之甚少，但質(zhì)譜鑒定表明，其能與SWC6形成復(fù)合體[75]。對(duì)SWC4的研究表明其參與植物雄配子和胚發(fā)育，且對(duì)葉片細(xì)胞的分化和伸長至關(guān)重要[75]，同時(shí)質(zhì)譜鑒定表明其與SWC6相互作用。利用SWC6-MYC融合蛋白進(jìn)行CoIP結(jié)合質(zhì)譜分析，SWC6與PIE1、SWC2、SWC4、YAF9A、RVB1、RVB2A、RVB2B、ARP4和ARP6形成復(fù)合體[75]，其pre-messenger RNA通過Ski- interacting protein (SKIP)介導(dǎo)剪切調(diào)控、和表達(dá)參與植物開花時(shí)間決定[78]。ARP6除與PIE1和SWC6相互作用參與PIE1和SWC6相似功能外，還通過促進(jìn)(DISRUPTED MEIOTIC cDNA1)表達(dá)促進(jìn)雌配子的減數(shù)分裂[79], 進(jìn)一步研究表明該過程是細(xì)胞色素P450基因(KLUH/ CYP78A5)通過促進(jìn)表達(dá)而實(shí)現(xiàn)[80]。

擬南芥中有2個(gè)與酵母INO80/SWR1復(fù)合體亞基Yaf9同源的基因：和。和在功能上有部分冗余，其中能與SWC6相互作用，且通過提高組蛋白H4乙?；酱龠M(jìn)其表達(dá)，從而降低和表達(dá), 抑制開花[81]。最新的研究表明，和通過調(diào)節(jié)細(xì)胞伸長和分化來影響植株發(fā)育, 且其調(diào)控開花還存在一條獨(dú)立于的途徑[82], 雖然YAF9s可通過維持(并不促進(jìn)) H2A.Z變體與基因區(qū)的結(jié)合和組蛋白H4乙酰化水平直接促進(jìn)表達(dá)[82]。

2.3 CHD復(fù)合體

基因家族成員在結(jié)構(gòu)上除含有DEAD/H- related ATP酶結(jié)構(gòu)域外，其N端還含有一段串聯(lián)chromodomains結(jié)構(gòu)域。所有CHD蛋白分為3類:CHD1和CHD2在C端含有DNA結(jié)合區(qū)；CHD3和CHD4的C端缺少DNA結(jié)合區(qū)，其N端有一對(duì)PHD結(jié)構(gòu)；CHD5~CHD9的C端含有多余結(jié)構(gòu)。酵母基因組僅編碼1個(gè)CHD蛋白CHD1，其可與組蛋白乙酰轉(zhuǎn)移酶復(fù)合體的(SAGA and SLIK complexes)亞基相互作用，并通過其PHD結(jié)構(gòu)域識(shí)別H3K4me3位點(diǎn)并與轉(zhuǎn)錄激活區(qū)結(jié)合促進(jìn)下游基因轉(zhuǎn)錄延伸和剪切。

除催化亞基外，對(duì)擬南芥CHD復(fù)合體的其他亞基我們還知之甚少。擬南芥基因組編碼4個(gè)CHD類催化亞基，分別為CHR5、PICKLE/CHR6、CHR4和CHR7。其中CHR5通過改變核小體“構(gòu)象”正調(diào)控表達(dá)參與植物抗病過程[84]。在種子發(fā)育過程CHR5通過結(jié)合于和啟動(dòng)子促進(jìn)二者表達(dá)，調(diào)控胚的發(fā)育[83]。有意思的是，在這個(gè)過程PICKLE拮抗CHR5的功能[83]，這也與PICKLE在萌發(fā)階段抑制種子胚性功能一致[112]。與AtBRM相似，PICKLE通過與拮抗PcG蛋白CLF (CURLY LEAF)的功能促進(jìn)主根中分生組織的活性[83]，而通過IAA14介導(dǎo)抑制側(cè)根起始基因和表達(dá)抑制側(cè)根的起始[86]。除在根中外, PICKLE還在葉片和花器官的發(fā)育過程拮抗CLF, 使其調(diào)控基因水平降低[113]。然而在14 d的幼苗中, PICKLE卻促進(jìn)其調(diào)控基因表達(dá)水平[87]，這提示在植物不同的發(fā)育階段PICKLE的功能不一樣。進(jìn)一步研究表明，PICKLE可與MADS-Box轉(zhuǎn)錄因子SEP3相互作用，提示在PICKLE影響花器官發(fā)育可能還依賴于SEP3[90]。PICKLE通過影響孢子體和配子體發(fā)育，調(diào)控植物的生殖生長[114]，而HY5通過招募PICKLE提高下游細(xì)胞伸長基因H3K27me3水平抑制其表達(dá)，從而抑制下胚軸伸長[91]。另外, PICKLE分別通過與PIF3、BZR1和DELLAs相互作用參與暗形態(tài)建成、BR和GA信號(hào)傳導(dǎo)過程[93], 從而將后三者整合在一起。進(jìn)一步研究表明, PICKLE通過抑制DELLAs的活性參與植物生長發(fā)育階段的轉(zhuǎn)化[89]。除GA信號(hào)外，PICKLE還通過直接促進(jìn)/的H3K27me3水平抑制其表達(dá)從而促進(jìn)植物營養(yǎng)階段轉(zhuǎn)變(vegetative phase change)(從童年到成熟)[90]。除調(diào)控H3K27me3水平外, PICKLE還通過參與RNA指導(dǎo)的DNA甲基化(RdDM, RNA-directed DNA methylation)抑制下游基因表達(dá)[88]。

2.4 ISWI 復(fù)合體

ISWI蛋白(imitation SWI)最早從果蠅胚胎細(xì)胞提取的核小體重塑活性過程中分離鑒定的，其為一類DEAD/H-related ATP酶，且還含有SANT和SLIDE結(jié)構(gòu)域。在體外加入模板，果蠅ISWI復(fù)合體促進(jìn)轉(zhuǎn)錄，而在體內(nèi)ISWI復(fù)合體亞基突變穩(wěn)定抑制同源基因(homeotic gene)表達(dá)。目前對(duì)植物ISWI類復(fù)合體的組成還知之甚少，對(duì)催化亞基的研究表明其參與多種生理過程。其中CHR11和CHR17通過共同調(diào)控基因區(qū)(gene body)核小體之間的“距離”(nucleosome spacing)調(diào)節(jié)下游基因表達(dá)[99]。同時(shí)CHR11和CHR17還分別通過與含DDT結(jié)構(gòu)域蛋白R(shí)INGLET1 (RLT1)和RLT2相互作用調(diào)控開花時(shí)間和花器官發(fā)育[100]。對(duì)該家族另一個(gè)成員DECREASE IN DNA METHYLATION 1 (DDM1)的研究表明，其主要參與DNA的甲基化過程。DDM1通過與Methyl- CpG binding domains (MBDs)相互作用改變后者在染色質(zhì)上的定位影響DNA的甲基化[94]，而一般認(rèn)為MBDs通過影響組蛋白的甲基化參與DNA的甲基化。與RdDM不同，DDM1參與的DNA甲基化主要由DNA甲基轉(zhuǎn)移酶CMT2介導(dǎo)[95]，二者通過提高異染色質(zhì)基因(如)不同區(qū)段的DNA甲基化水平維持基因沉默。事實(shí)上, DDM1是通過影響異染色質(zhì)H1構(gòu)象使CMT2更加容易結(jié)合于異染色質(zhì)DNA而實(shí)現(xiàn)DNA甲基化修飾的[95]。進(jìn)一步研究表明，DDM1還可促進(jìn)甲基化的DNA在核小體上纏繞形成更為緊密的染色質(zhì)結(jié)構(gòu)[96]。有意思的是,突變體在連續(xù)種植5代內(nèi)，其端粒大小與野生型相似，而在第6和以后的世代中端粒大小顯著減小[97]，這似乎說明在介導(dǎo)的端粒維持有一定的時(shí)間劑量效應(yīng)。同時(shí)突變體亦出現(xiàn)葉片延遲衰老的表型，提示還參與葉片發(fā)育，然而對(duì)于具體機(jī)制仍不清楚[98]。

2.5 其他Snf2-like蛋白

目前對(duì)其他Snf2-like蛋白的功能還不是十分清楚，根據(jù)同源性分析這些蛋白(41個(gè)中的大部分)并不能歸于以上復(fù)合體中的任意一種。但通過突變體表型分析表明某些成員也有重要的功能。Rad54- like家族成員DRD1/CHR35 (DEFECTIVE IN RNA- DIRECTED DNA METHYLATION1)與RDM1 (RNA-DIRECTED DNA METHYLATION 1)和DMS3 (DEFECTIVE IN MERISTEM SILENCIN G3)形成復(fù)合體(DDR complex)，通過polymerase V介導(dǎo)參與RdDM[101]。而該家族另一成員Rad54/CHR25則通過同源重組途徑參與DNA的修復(fù)[102]。

與擬南芥相比，其他物種僅有少數(shù)Snf2-like蛋白被研究。如水稻()同源基因和也參與DNA的甲基化[115]，而CHD3家族成員通過GA信號(hào)途徑調(diào)控水稻幼苗發(fā)育[116]。小番茄(‘Micro-Tom’)過表達(dá)基因()可抑制生長發(fā)育[117]。

3 結(jié)語

染色質(zhì)重塑作為表觀遺傳調(diào)控的重要內(nèi)容在真核生物DNA復(fù)制、轉(zhuǎn)錄、重組和DNA修復(fù)等過程中起到重要的作用。對(duì)植物染色質(zhì)重塑復(fù)合體亞基(染色質(zhì)重塑因子)的研究表明，它們參與細(xì)胞分化、器官發(fā)育和激素信號(hào)轉(zhuǎn)導(dǎo)等多種生理過程。然而相對(duì)于酵母和動(dòng)物，植物染色質(zhì)重塑的研究還相對(duì)滯后，其作用機(jī)制并不十分清楚，最主要的問題是植物染色質(zhì)重塑是如何識(shí)別其作用位點(diǎn)的。在酵母和動(dòng)物中的研究結(jié)果表明該過程與組蛋白的修飾有關(guān)，這就為我們后續(xù)研究植物染色質(zhì)重塑和組蛋白修飾之間的Cross-Talk指明了方向。同時(shí)綜上所述，染色質(zhì)重塑因子在不同的發(fā)育(或基因調(diào)節(jié))過程與不同的因子(包括轉(zhuǎn)錄因子和核蛋白等)相互作用以及染色質(zhì)重塑因子的翻譯后修飾將極大拓展其調(diào)控基因表達(dá)的內(nèi)涵。

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Functions of ATP-dependent Chromatin Remodeling Factors in Plant Development

PENG Xiu-ling1,2, WANG Jian-hao1,2, YANG Song-guang1*

(1. Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China; 2.University of Chinese Academy of Sciences, Chinese Academy of Sciences,Beijing 100049, China)

In eukaryotic cells, the ATP-dependent chromatin remodeling complexes utilize the energy of ATP to disrupt nucleosome DNA contacts, move nucleosomes along DNA, and remove or exchange nucleosomes. They thus make DNA/chromatin available to proteins that need to access DNA or histones directly during cellular processes. The first chromatin remodeling complex was found in yeast, containing at least 11 subunits by biochemical analysis. However, the chromatin remodeling complexes in plants are less known. The studies on plant chromatin remodeling factors were reviewed, which would provide insights into the involvement of plant chromatin remodeling in development.

Chromatin remodeling factor; Epigenetic regulation; Function; Plant

10.11926/jtsb.4070

2019–03–25

2019–05–17

廣東省杰出青年基金項(xiàng)目(2016A030306047); 廣州市珠江科技新星項(xiàng)目(201610010138); 國家自然科學(xué)基金項(xiàng)目(31672161)資助

This work was supported by the Guangdong Natural Science Funds for Distinguished Young Scholars (Grant No. 2016A030306047); the Pearl River Science and Technology Nova Program of Guangzhou (Grant No. 201610010138), and the National Natural Science Foundation of China (Grant No. 31672161).

E-mail: yangsongguang@scbg.ac.cn